Mobile antibiotic resistance – the spread of genes determining the resistance of bacteria through food products
Jolanta Godziszewska 1 , Dominika Guzek 1 , Krzysztof Głąbski 2 , Agnieszka Wierzbicka 1Abstract
In recent years, more and more antibiotics have become ineffective in the treatment of bacterial nfections. The acquisition of antibiotic resistance by bacteria is associated with circulation of genes in the environment. Determinants of antibiotic resistance may be transferred to pathogenic bacteria. It has been shown that conjugation is one of the key mechanisms responsible for spread of antibiotic resistance genes, which is highly efficient and allows the barrier to restrictions and modifications to be avoided. Some conjugative modules enable the transfer of plasmids even between phylogenetically distant bacterial species. Many scientific reports indicate that food is one of the main reservoirs of these genes. Antibiotic resistance genes have been identified in meat products, milk, fruits and vegetables. The reason for such a wide spread of antibiotic resistance genes is the overuse of antibiotics by breeders of plants and animals, as well as by horizontal gene transfer. It was shown, that resistance determinants located on mobile genetic elements, which are isolated from food products, can easily be transferred to another niche. The antibiotic resistance genes have been in the environment for 30 000 years. Their removal from food products is not possible, but the risks associated with the emergence of multiresistant pathogenic strains are very large. The only option is to control the emergence, selection and spread of these genes. Therefore measures are sought to prevent horizontal transfer of genes. Promising concepts involve the combination of developmental biology, evolution and ecology in the fight against the spread of antibiotic resistance.
References
- 1. Aarestrup F.: Get pigs off antibiotics. Nature, 2012; 486: 465-466
Google Scholar - 2. Alippi A.M., León I.E., López A.C.: Tetracycline-resistance encodingplasmids from Paenibacillus larvae, the causal agent of Americanfoulbrood disease, isolated from commercial honeys. Int. Microbiol.,2014; 17: 49-61
Google Scholar - 3. Baj J., Markiewicz Z.: Biologia molekularna bakterii. WydawnictwoNaukowe PWN, Warszawa, 2006
Google Scholar - 4. Baquero F., Coque T.M., de la Cruz F.: Ecology and evolution as targets:the need for novel eco-evo drugs and strategies to fight antibioticresistance. Antimicrob. Agents Chemother., 2011; 55: 3649-3660
Google Scholar - 5. Bonyadian M., Moshtaghi H., Akhavan T.M.: Molecular characterizationand antibiotic resistance of enterotoxigenic and enteroaggregativeEscherichia coli isolated from raw milk and unpasteurizedcheeses. Vet. Res. Forum, 2014; 5: 29-34
Google Scholar - 6. Chajęcka-Wierzchowska W., Zadernowska A., Nalepa B., SierpińskaM., Łaniewska-Trokenheim Ł.: Coagulase-negative staphylococci(CoNS) isolated from ready-to-eat food of animal origin – phenotypicand genotypic antibiotic resistance. Food Microbiol., 2015;46: 222-226
Google Scholar - 7. Cook A., Reid-Smith r.J., Irwin r.J., McEwen S.A., Young V., Butt K.,Ribble C.: Antimicrobial resistance in Escherichia coli isolated fromretail milk-fed veal meat from Southern Ontario, Canada. J. FoodProt., 2011; 74: 1328-1333
Google Scholar - 8. D’Costa V.M., King C.E., Kalan L., Morar M., Sung W.W., SchwarzC., Froese D., Zazula G., Calmels F., Debruyne r., Golding G.B., PoinarH.N., Wright G.D.: Antibiotic resistance is ancient. Nature, 2011;477: 457-461
Google Scholar - 9. de Neeling A.J., van den Broek M.J., Spalburg E.C., van SantenVerheuvelM.G., Dam-Deisz W.D., Boshuizen H.C., van de Giessen A.W.,van Duijkeren E., Huijsdens X.W.: High prevalence of methicillin resistantStaphylococcus aureus in pigs. Vet. Microbiol., 2007; 122: 366-372
Google Scholar - 10. Fernandez-Lopez r., Machón C., Longshaw C.M., Martin S., MolinS., Zechner E.L., Espinosa M., Lanka E., de la Cruz F.: Unsaturatedfatty acids are inhibitors of bacterial conjugation. Microbiology,2005; 151: 3517-3526
Google Scholar - 11. Fessler A.T., Olde Riekerink r.G., Rothkamp A., Kadlec K., SampimonO.C., Lam T.J., Schwarz S.: Characterization of methicillinresistantStaphylococcus aureus CC398 obtained from humans andanimals on dairy farms. Vet. Microbiol; 2012; 160: 77-84
Google Scholar - 12. Garcillán-Barcia M.P., Jurado P., González-Pérez B., Moncalián G.,Fernández L.A., de la Cruz F.: Conjugative transfer can be inhibitedby blocking relaxase activity within recipient cells with intrabodies.Mol. Microbiol., 2007; 63: 404-416
Google Scholar - 13. Gundogan N., Citak S., Yucel N., Devren A.: A note on the incidenceand antibiotic resistance of Staphylococcus aureus isolated frommeat and chicken samples. Meat Sci., 2005; 69: 807-810
Google Scholar - 14. IDSA Eduction & Research Foundation.: Antibiotic Resistance.http://www.idsociety.org/uploadedFiles/IDSA/Policy_and_Advocacy/Current_Topics_and_Issues/Antimicrobial_Resistance/WHD/Antibiotic%20Resistance%20Fact%20Sheet%281%29.pdf (10.04.2015)
Google Scholar - 15. Jahan M., Zhanel G.G., Sparling r., Holley r.A.: Horizontal transferof antibiotic resistance from Enterococcus faecium of fermentedmeat origin to clinical isolates of Enterococcus faecium and Enterococcusfaecalis. Int. J. Food Microbiol., 2015; 199: 78-85
Google Scholar - 16. Jarmuła A, Obłąk E, Wawrzycka D, Gutowicz J.: Efflux-mediatedantimicrobial multidrug resistance. Postępy Hig. Med. Dośw. 2011;65: 216-227
Google Scholar - 17. Johnsborg O., Eldholm V., Håvarstein L.S.: Natural genetic transformation:prevalence, mechanisms and function. Res. Microbiol.,2007; 158: 767-778
Google Scholar - 18. Kitai S., Shimizu A., Kawano J., Sato E., Nakano C., Uji T., KitagawaH.: Characterization of methicillin-resistant Staphylococcus aureusisolated from retail raw chicken meat in Japan. J. Vet. Med. Sci.,2005; 67: 107-110
Google Scholar - 19. Kreausukon K., Fetsch A., Kraushaar B., Alt K., Müller K., KrömkerV., Zessin K.H., Käsbohrer A., Tenhagen B.A.: Prevalence, antimicrobialresistance, and molecular characterization of methicillinresistantStaphylococcus aureus from bulk tank milk of dairy herds. J.Dairy Sci., 2012; 95: 4382-4388
Google Scholar - 20. Kwon N.H., Park K.T., Jung W.K., Youn H.Y., Lee Y., Kim S.H., BaeW., Lim J.Y., Kim J.Y., Kim J.M., Hong S.K., Park Y.H.: Characteristicsof methicillin resistant Staphylococcus aureus isolated from chickenmeat and hospitalized dogs in Korea and their epidemiological relatedness.Vet. Microbiol., 2006; 117: 304-312
Google Scholar - 21. Lawley T.D., Gordon G.S., Wright A., Taylor D.E.: Bacterial conjugativetransfer: visualization of successful mating pairs and plasmidestablishment in live Escherichia coli. Mol. Microbiol., 2002; 44:947-956
Google Scholar - 22. Lee J.: Occurrence of methicillin-resistant Staphylococcus aureusstrains from cattle and chicken, and analyses of their mecA, mecR1and mecI genes. Vet. Microbiol., 2006; 114: 155-159
Google Scholar - 23. Lin A., Jimenez J., Derr J., Vera P., Manapat M.L., Esvelt K.M.,Villanueva L., Liu D.R., Chen I.A.: Inhibition of bacterial conjugationby phage M13 and its protein g3p: quantitative analysis and model.PLoS One, 2011; 6: e19991
Google Scholar - 24. Ling L.L., Schneider T., Peoples A.J., Spoering A.L., Engels I.,Conlon B.P., Mueller A., Schäberle T.F., Hughes D.E., Epstein S., JonesM., Lazarides L., Steadman V.A., Cohen D.R., Felix C.R. i wsp.: A newantibiotic kills pathogens without detectable resistance. Nature,2015; 517: 455-459
Google Scholar - 25. Llor C., Bjerrum L.: Antimicrobial resistance: risk associated withantibiotic overuse and initiatives to reduce the problem. Ther. Adv.Drug Saf., 2014; 5: 229-241
Google Scholar - 26. Lorenz M.G., Wackernagel W.: Bacterial gene transfer by naturalgenetic transformation in the environment. Microbiol. Rev., 1994;58: 563-602
Google Scholar - 27. Lujan S.A., Guogas L.M., Ragonese H., Matson S.W., RedinboM.R.: Disrupting antibiotic resistance propagation by inhibitingthe conjugative DNA relaxase. Proc. Natl. Acad. Sci. USA, 2007; 104:12282-12287
Google Scholar - 28. Markiewicz Z., Kwiatkowski A.A.: Bakterie, antybiotyki, lekooporność.Wydawnictwo Naukowe PWN, Warszawa 2006
Google Scholar - 29. McEachran A.D., Blackwell B.R., Hanson J.D., Wooten K.J., MayerG.D., Cox S.B., Smith P.N.: Antibiotics, bacteria, and antibiotic resistancegenes: aerial transport from cattle feed yards via particulatematter. Environ. Health Perspect., 2015; 123: 337-343
Google Scholar - 30. McGhee G.C., Guasco J., Bellomo L.M., Blumer-Schuette S.E., ShaneW.W., Irish-Brown A., Sundin G.W.: Genetic analysis of streptomycinresistant(SmR) strains of Erwinia amylovora suggests that disseminationof two genotypes is responsible for the current distribution of SmR E.amylovora in Michigan. Phytopathology, 2011; 101: 182-191
Google Scholar - 31. Mole B.: MRSA: farming up trouble. Nature, 2013; 499: 398-400
Google Scholar - 32. Morar A., Sala C., Imre K.: Occurrence and antimicrobial susceptibilityof Salmonella isolates recovered from the pig slaughterprocess in Romania. J. Infect. Dev. Ctries., 2015; 9: 99-104
Google Scholar - 33. Morar M., Wright G.D.: The genomic enzymology of antibioticresistance. Annu. Rev. Genet., 2010; 44: 25-51
Google Scholar - 34. Muschiol S., Balaban M., Normark S., Henriques-Normark B.: Uptakeof extracellular DNA: Competence induced pili in natural transformationof Streptococcus pneumoniae. Bioessays, 2015; 37: 426-435
Google Scholar - 35. Normanno G., Corrente M., La Salandra G., Dambrosio A., QuagliaN.C., Parisi A., Greco G., Bellacicco A.L., Virgilio S., Celano G.V.:Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animalorigin product in Italy. Int. J. Food Microbiol., 2007; 117: 219-222
Google Scholar - 36. Peles F., Wagner M., Varga L., Hein I., Rieck P., Gutser K., KeresztúriP., Kardos G., Turcsányi I., Béri B., Szabó A.: Characterization ofStaphylococcus aureus strains isolated from bovine milk in Hungary.Int. J. Food Microbiol., 2007; 118: 186-193
Google Scholar - 37. Pereira V., Lopes C., Castro A., Silva J., Gibbs P., Teixeira P.: Characterizationfor enterotoxin production, virulence factors, and antibioticsusceptibility of Staphylococcus aureus isolates from variousfoods in Portugal. Food Microbiol., 2009; 26: 278-282
Google Scholar - 38. Phillips I.: Withdrawal of growth-promoting antibiotics in Europeand its effects in relation to human health. Int. J. Antimicrob.Agents, 2007; 30: 101-107
Google Scholar - 39. Rozporządzenie Ministra Rolnictwa i Rozwoju Wsi z dnia 20marca 2003 r. w sprawie badań kontrolnych pozostałości chemicznych,biologicznych, leków i skażeń promieniotwórczych u zwierzątżywych, w tkankach lub narządach zwierząt po uboju i w produktachspożywczych pochodzenia zwierzęcego. Dz. U., 31 marca 2003
Google Scholar - 40. Skočková A., Bogdanovičová K., Koláčková I., Karpíšková r.: Antimicrobialresistant and extended Spectrum β-lactamase producingEscherichia coli in raw cow’s milk. J. Food Prot., 2015; 78: 72-77
Google Scholar - 41. Smillie C., Garcillán-Barcia M.P., Francia M.V., Rocha E.P., de laCruz F.: Mobility of plasmids. Microbiol. Mol. Biol. Rev., 2010; 74:434-452
Google Scholar - 42. Smith K.P., Kumar S., Varela M.F.: Identification, cloning, andfunctional characterization of EmrD-3, a putative multidrug effluxpump of the major facilitator superfamily from Vibrio cholerae O395.Arch. Microbiol., 2009; 191: 903-911
Google Scholar - 43. Stockwell V.O., Duffy B.: Use of antibiotic in plant agriculture.Rev. Sci. Tech., 2012; 31: 199-210
Google Scholar - 44. Valenzuela A.S., Benomar N., Abriouel H., Cañamero M.M.,Gálvez A.: Isolation and identification of Enterococcus faecium fromseafoods: antimicrobial resistance and production of bacteriocinlikesubstances. Food Microbiol., 2010; 27: 955-961
Google Scholar - 45. Virge H.: Effects of the termination of antibiotic growth promotersuse on antimicrobial resistance in pig farms: Macrolide-resistanceamong enterococci in finishers. DIAS report. Animal Husbandry,2004; 57: 29-33
Google Scholar - 46. Wang N., Yang X., Jiao S., Zhang J., Ye B., Gao S.: Sulfonamideresistantbacteria and their resistance genes in soils fertilized withmanures from Jiangsu Province, Southeastern China. PLoS One, 2014;9: e112626
Google Scholar - 47. Wojtasik-Kalinowska I., Konarska M., Sakowska A., Guzek D.,Głąbska D., Wierzbicka A.: Sektor mięsa wieprzowego w Polsce i naświecie w latach 2000-2012. Zeszyty Naukowe Szkoły Głównej GospodarstwaWiejskiego w Warszawie, 2014; 3: 205-215
Google Scholar - 48. Wright G.D.: Making sense of antisense in antibiotic drug discovery.Cell Host Microbe, 2009; 6: 197-198
Google Scholar